diff --git a/src/plugins/contracts/run-context-lifecycle.contract.test.ts b/src/plugins/contracts/run-context-lifecycle.contract.test.ts
index b6bf48f8d96..0f2148b563e 100644
--- a/src/plugins/contracts/run-context-lifecycle.contract.test.ts
+++ b/src/plugins/contracts/run-context-lifecycle.contract.test.ts
@@ -315,6 +315,94 @@ describe("plugin run context lifecycle", () => {
     ).toBeUndefined();
   });
 
+  it("waits for terminal handlers added after the first terminal cleanup waiter starts", async () => {
+    let releaseFirstTerminalHandler: (() => void) | undefined;
+    let releaseSecondTerminalHandler: (() => void) | undefined;
+    let firstTerminalHandlerSawContext: unknown;
+    let secondTerminalHandlerSawContext: unknown;
+    let terminalEventsSeen = 0;
+    const { config, registry } = createPluginRegistryFixture();
+    registerTestPlugin({
+      registry,
+      config,
+      record: createPluginRecord({
+        id: "repeated-terminal-live-wait",
+        name: "Repeated Terminal Live Wait",
+      }),
+      register(api) {
+        api.registerAgentEventSubscription({
+          id: "records",
+          streams: ["tool", "lifecycle"],
+          async handle(event, ctx) {
+            if (event.stream === "tool") {
+              ctx.setRunContext("seen", { runId: event.runId });
+              return;
+            }
+            if (event.data?.phase !== "end") {
+              return;
+            }
+            terminalEventsSeen += 1;
+            if (terminalEventsSeen === 1) {
+              await new Promise<void>((resolve) => {
+                releaseFirstTerminalHandler = resolve;
+              });
+              firstTerminalHandlerSawContext = ctx.getRunContext("seen");
+              return;
+            }
+            await new Promise<void>((resolve) => {
+              releaseSecondTerminalHandler = resolve;
+            });
+            secondTerminalHandlerSawContext = ctx.getRunContext("seen");
+          },
+        });
+      },
+    });
+    setActivePluginRegistry(registry.registry);
+
+    emitAgentEvent({
+      runId: "run-repeated-terminal-live-wait",
+      stream: "tool",
+      data: { name: "tool" },
+    });
+    await waitForPluginEventHandlers();
+
+    emitAgentEvent({
+      runId: "run-repeated-terminal-live-wait",
+      stream: "lifecycle",
+      data: { phase: "end" },
+    });
+    await waitForPluginEventHandlers();
+
+    emitAgentEvent({
+      runId: "run-repeated-terminal-live-wait",
+      stream: "lifecycle",
+      data: { phase: "end" },
+    });
+    await waitForPluginEventHandlers();
+
+    releaseFirstTerminalHandler?.();
+    await waitForPluginEventHandlers();
+    expect(firstTerminalHandlerSawContext).toEqual({ runId: "run-repeated-terminal-live-wait" });
+    expect(
+      getPluginRunContext({
+        pluginId: "repeated-terminal-live-wait",
+        get: { runId: "run-repeated-terminal-live-wait", namespace: "seen" },
+      }),
+    ).toEqual({ runId: "run-repeated-terminal-live-wait" });
+
+    releaseSecondTerminalHandler?.();
+    await waitForPluginEventHandlers();
+    await waitForPluginEventHandlers();
+
+    expect(secondTerminalHandlerSawContext).toEqual({ runId: "run-repeated-terminal-live-wait" });
+    expect(
+      getPluginRunContext({
+        pluginId: "repeated-terminal-live-wait",
+        get: { runId: "run-repeated-terminal-live-wait", namespace: "seen" },
+      }),
+    ).toBeUndefined();
+  });
+
   it("clears run context after the terminal subscription grace period", async () => {
     vi.useFakeTimers();
     let releaseTerminalHandler: (() => void) | undefined;
diff --git a/src/plugins/host-hook-runtime.ts b/src/plugins/host-hook-runtime.ts
index fbd78333d89..0a14c290b51 100644
--- a/src/plugins/host-hook-runtime.ts
+++ b/src/plugins/host-hook-runtime.ts
@@ -107,16 +107,20 @@ function trackAgentEventHandler(runId: string, pending: Promise<void>): void {
   });
 }
 
-function waitForTerminalEventHandlers(params: {
-  runId: string;
-  pendingHandlers: Set<Promise<void>>;
-}): Promise<void> {
-  const { pendingHandlers, runId } = params;
-  if (pendingHandlers.size === 0) {
-    return Promise.resolve();
+async function waitForLiveTerminalEventHandlers(runId: string): Promise<"settled"> {
+  for (;;) {
+    const pendingHandlers = getPluginHostRuntimeState().pendingAgentEventHandlersByRunId.get(runId);
+    if (!pendingHandlers || pendingHandlers.size === 0) {
+      return "settled";
+    }
+    await Promise.allSettled(pendingHandlers);
   }
+}
+
+function waitForTerminalEventHandlers(params: { runId: string }): Promise<void> {
+  const { runId } = params;
   let timeout: NodeJS.Timeout | undefined;
-  const settled = Promise.allSettled(pendingHandlers).then(() => "settled" as const);
+  const settled = waitForLiveTerminalEventHandlers(runId);
   // Promise.race bounds the host wait; JavaScript cannot cancel the plugin
   // promises themselves, so timeout also marks the run expired to block late
   // run-context resurrection by handlers that eventually settle.
@@ -340,12 +344,8 @@ export function dispatchPluginAgentEventSubscriptions(params: {
   }
   if (isTerminalEvent) {
     markPluginRunClosed(params.event.runId);
-    const pendingForRun =
-      getPluginHostRuntimeState().pendingAgentEventHandlersByRunId.get(params.event.runId) ??
-      new Set(pendingHandlers);
     void waitForTerminalEventHandlers({
       runId: params.event.runId,
-      pendingHandlers: new Set(pendingForRun),
     }).then(() => {
       clearPluginRunContext({ runId: params.event.runId });
     });